MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 523: 199–213, 2015
doi: 10.3354/meps11130
Published March 16
Factors driving Adélie penguin chick size,
mass and condition at colonies of different sizes in
the Southern Ross Sea
Amy L. Whitehead1, 8, Phil O’B. Lyver1, Grant Ballard2, Kerry Barton3, Brian J. Karl1,
Katie M. Dugger4, 9, Scott Jennings4, Amelie Lescroël5, Peter R. Wilson6,
David G. Ainley7,*
1
Landcare Research, PO Box 69040, Lincoln 7640, New Zealand
2
Point Blue Conservation Science, 3820 Cypress Drive, Petaluma, California 94954, USA
3
BartonK Solutions, 11 Thompson Terrace, Nelson 7010, New Zealand
4
Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon 97331-3803, USA
5
CEFE UMR 5175, CNRS - Université de Montpellier - Université Paul-Valéry Montpellier − EPHE, 1919 route de Mende,
34293 Montpellier cedex 5, France
6
St Heliers, Auckland, New Zealand
H. T. Harvey and Associates, 983 University Avenue, Los Gatos, California 95032, USA
7
8
Present address: Quantitative and Applied Ecology Group, School of Botany, University of Melbourne, Parkville,
Victoria 3010, Australia
9
Present address: US Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit,
Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon 97331-3803, USA
ABSTRACT: Body size, mass and condition can affect an organism’s ability to cope with variation
in resource availability or metabolic demand, particularly as juveniles reach independence. It
follows that changes to parental provisioning efficiency (size and frequency of meals) through
intraspecific competition or environmental conditions that affect prey availability may affect chick
size, mass and condition and ultimately post-fledging survival. We examined how Adélie penguin
chick size, mass and condition varied among colonies of different sizes on Ross Island during a
15 yr period of high environmental variability and varying intraspecific competition. Aiding the
study was a natural experiment in which the presence of 2 giant icebergs midway through the
study abnormally increased sea ice concentration (SIC), altering adults’ access to food. Concurrently, the colonies were rapidly increasing in size; based on previous work, this indicated
increased trophic competition near colonies, a trend likely indicating a changing food web in the
greater region. Results showed that increased amounts of sea ice, which reduced the ability of
adults to access food, had a negative effect on the size and mass of chicks. However, a greater proportion of fish (vs. krill) in the diet had a positive effect on chick size. Moreover, in some cases,
increased intraspecific competition may be a more important driver of provisioning rate and chick
size than abiotic factors, with chicks showing the effects of reduced food delivery at larger
colonies. Understanding these patterns will allow better understanding of how factors such as
climate change and altered food webs may affect Adélie penguin populations.
KEY WORDS: Adélie penguin · Chick growth · Diet variability · Provisioning efficiency ·
Intraspecific competition
Resale or republication not permitted without written consent of the publisher
*Corresponding author: dainley@penguinscience.com
© Inter-Research 2015 · www.int-res.com
Mar Ecol Prog Ser 523: 199–213, 2015
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INTRODUCTION
Energy reserves, as judged by the ratio of body
mass to body size, may be important determinants of
an organism’s potential fitness and ultimately affect
survivorship (Schulte-Hostedde et al. 2005). A high
body mass or good condition may buffer against periods of low resource availability or high metabolic
demand, enabling individuals to use stored energy
reserves to survive short periods of stress (Ballard et
al. 2010). Such effects may be particularly important
for naïve juveniles when they first become independent of their parents and must learn to forage for
themselves (Stienen & Brenninkmeijer 2002). In such
situations, young that have a high body mass and/or
are in good condition may be expected to have
higher survival rates, and therefore be more likely to
recruit into the breeding population (Sagar & Horning 1998, Kitaysky et al. 2006).
Body condition is likely to be strongly influenced
by a range of abiotic (Schreiber 2001) and biotic (Lilliendahl 1998, Wanless et al. 2005) factors. For example, variable climatic regimes may be metabolically
costly, with individuals using proportionally more
energy for body maintenance and survival, thus
reducing the energy that can be allocated to growth
(Yoda & Ropert-Coudert 2007, Chapman et al. 2011).
Periods of environmental perturbation may also
change patterns of prey abundance, quality or accessibility, leading to reduced foraging efficiency (Ballard et al. 2010, Lescroël et al. 2010, 2014). Finally,
reduction in the prevalence of both inter- and intraspecific trophic competitors can lead to increased
availability of prey and thus increased foraging efficiency (Ainley et al. 2004, 2006, 2007, Lyver et al.
2011, Trathan et al. 2012). As noted in those studies
and expanded below, changes in colony size as well
as the increased prevalence of marine mammals foraging on the same prey can negatively alter provisioning efficiency (the amount of food delivered to
chicks per unit time) and colony productivity.
Reduced provisioning efficiency has been shown to
negatively impact chick meal sizes, chick growth,
and fledging mass in some seabird species (e.g. Cruz
& Cruz 1990, Williams & Croxall 1990, Wanless et al.
2005, Ballard et al. 2010) as adults prioritise selfmaintenance over chick provisioning. However,
there is also evidence that some species are able to
compensate for stressful conditions by modifying
adult or chick behaviours to maximise the benefits of
available resources (Weimerskirch et al. 1995,
Waugh et al. 2000, Ballard et al. 2010). Individuals
may alter the timing of breeding, switch to alternate
prey or change the timing or frequency at which
chicks are fed to buffer the effects of environmental
stress (Vinuela et al. 1996, Salihoglu et al. 2001,
Chapman et al. 2011).
The foraging efficiency of Adélie penguins Pygoscelis adeliae is strongly influenced by changes in
environmental conditions, particularly the sea ice
concentration (SIC) within their foraging area
(Emmerson & Southwell 2008, Ballard et al. 2010,
Lescroël et al. 2010, 2014, Cottin et al. 2012). Adélie
penguins are sea ice obligates, generally existing in
areas of intermediate SIC where there is adequate
ice for resting and facilitating the ice-associated food
web, but not so much that individuals incur additional energetic cost associated with walking great
distances between colonies and foraging areas (Ainley 2002, Emmerson & Southwell 2008). Indeed, adult
Adélie penguins on Ross Island exhibit longer foraging trips and deliver less food to their chicks during periods of high SIC as a result of reduced access
to prey (Ballard et al. 2010). Adélie penguin diet
composition also varies with SIC, as crystal krill
Euphausia crystallorophias are more prevalent than
subadult silverfish Pleuragramma antarcticum when
SIC is high (Ainley et al. 2003). Adult krill typically
have a lower calorific value than subadult silverfish,
which may further exacerbate the effects of reduced
provisioning efficiency during periods of high SIC
(Ainley et al. 2003).
Inter- and intraspecific competition can also affect
prey availability to penguins. Parents make increasingly longer foraging trips throughout the breeding
season at large colonies due to progressive prey
depletion (Ainley et al. 2004, Ballance et al. 2009,
Ford et al. 2014). Similarly, the arrival of cetaceans in
the foraging areas correlates with longer penguin
foraging trips as well as changes in penguin diet
(Ainley et al. 2006). Finally, the removal of trophic
competitors, such as minke whales Balaenoptera
bonaerensis and more recently Antarctic toothfish
Dissostichus mawsoni, correlates with periods of
increased Adélie penguin population growth (Ainley
et al. 2007, 2013, Lyver et al. 2014).
It has also been shown that Adélie penguin adults,
particularly those beginning the breeding season in
relatively better condition, may allocate a greater
proportion of captured prey toward chick provisioning than to their own needs and thus sacrifice their
own condition in favour of chick growth (Salihoglu et
al. 2001, Ballard et al. 2010). Adults may alter the frequency of food delivery and food quality, while
chicks can adjust metabolic processes to match provisioning rates (Salihoglu et al. 2001). Indeed, fledg-
Whitehead et al.: Factors affecting Adélie penguin chicks
ing mass of Adélie penguin chicks (2.8 to 3.2 kg) from
colonies around Anvers Island, Antarctica, remained
relatively constant over 25 yr despite significant variability in the abundance of their primary prey resource, Antarctic krill Euphausia superba (Salihoglu
et al. 2001), indicating that compensatory mechanisms were likely important. In contrast, fledging
mass of chicks gradually decreased over a 15 yr
period at colonies farther north on the Antarctic
Peninsula, in association with decreasing Adélie
populations and a supposed decrease in krill availability (Hinke et al. 2007). The higher concentration
of fish in the Anvers Island penguins’ diet appeared
to be a compensatory factor in chick provisioning
(Chapman et al. 2011). Despite decreases in the population size of northern colonies, modelling has
shown that there was sufficient abundance of krill,
but perhaps not fish, necessary to maintain these
Adélie penguin colonies along the western Antarctic
Peninsula (Sailley et al. 2013).
In this study, we examined how Adélie penguin
chick size, mass and condition varied among 3
breeding colonies of different sizes on Ross Island
over 15 breeding seasons during a period of high
environmental variability. We hypothesised that
chick size, mass and condition would be dependent
on environmental conditions and the intraspecific
competition that adults experience while provisioning their chicks. Alternatively, the hypothesis that
chick size, mass, or condition do not vary with environmental conditions or competition would imply
that Adélie penguins are able to alter their chick provisioning behaviours and compensate for a wide
range of conditions, as has been shown previously
over shorter time periods (Salihoglu et al. 2001, Ballard et al. 2010). Herein, we follow Lewis et al. (2001)
and subsequent authors in defining intraspecific
competition as increased pressure on the availability
of prey as a function of inter- and intra-colony variation in size.
The presence of 2 giant icebergs (B-15 and C-16),
the largest the size of Jamaica, grounded off the
coast of Ross Island between January 2001 and July
2006 provided a large-scale ‘natural experiment.’
During this experiment, SIC increased to an unusual
degree within the summer foraging areas of 2 of the
colonies, where the SIC was already highly variable
(Fig. 1a); the foraging areas, location of icebergs, and
effect on SIC are shown by images in Dugger et al.
(2014) and Ford et al. (2014). At the third colony, the
presence of the giant icebergs precluded foraging
within the marginal ice zone (MIZ) of the Ross Sea
Polynya, a highly productive area (Ballard et al. 2010,
201
Dugger et al. 2014, Lescroël et al. 2014). In addition,
a fishery for Antarctic toothfish (a direct trophic competitor of Adélie penguins for silverfish) was initiated
in the first year of our study (peaking in catch around
2004, remaining relatively constant thereafter) and
corresponded with the disappearance of large fish in
southern Ross Sea waters (Ainley et al. 2013). We
investigated whether the size, mass and condition of
chicks varied with provisioning efficiency, diet composition (% fish), intraspecific competition among
parents (colony size), breeding output (no. of chicks
per pair), as well as abiotic environmental conditions
(iceberg presence, SIC). The present paper and that
by Dugger et al. (2014) are complementary, with the
present paper addressing in much greater detail the
subject of chick growth. We evaluated the following
3 general predictions, parsing each into specific predictions (see ‘Materials and methods’): (1) Chick size
and mass will be greater, and condition will be better, when provisioning efficiency is high, SIC is low,
and fish are dominant in the diet. (2) Chick size and
mass will be greater, and condition will be better, in
breeding seasons with low intraspecific resource
competition. We expect greater intraspecific resource competition among foraging parents to be
associated with large breeding populations and high
breeding output (more chicks produced per pair). (3)
Sibling chicks will be most similar in size, mass and
condition in breeding seasons with low intraspecific
resource competition (measured as in prediction 2).
Understanding the mechanisms that determine the
size, mass and condition of Adélie penguin chicks,
and thus their subsequent survival and recruitment,
will allow for better predictions of the future size and
distribution of Adélie penguin colonies under rapidly
changing environmental conditions in the Ross Sea
(Ainley et al. 2010).
MATERIALS AND METHODS
Field site
Fieldwork was conducted at Cape Royds (77° 34’ S,
166° 11’ E), Cape Bird (77° 13’ S, 166° 28’ E) and Cape
Crozier (77° 27’ S, 169° 23’ E) on Ross Island, southwestern Ross Sea (see maps in Ainley et al. 2004,
Shepherd et al. 2005, Ford et al. 2014). These
colonies comprise ~9% of the global Adélie penguin
population (Lynch & LaRue 2014) and vary in size by
3 orders of magnitude (range in number of breeding
pairs at each colony during this study: Cape Royds
1300 to 3900; Cape Bird 23 000 to 69 000; Cape
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Fig. 1. Mean annual trends in (a) sea ice concentration (SIC), (b) colony size and (c) breeding output for Adélie penguins at 3
colonies on Ross Island. Colony size data represent the relative change in the number of breeding pairs at a given colony relative to 1996, with colonies arranged in order of increasing size from left to right (size in 1996: Cape Royds = 3378, Cape Bird
= 33 286, Cape Crozier = 117 675 pairs). The presence of the giant icebergs is indicated by the shading. Error bars represent
standard errors. Further details on each of the metrics can be found in Table 1 and ‘Materials and methods’
Crozier 67 000 to 282 000; Fig. 1b, see also Lyver et al.
2014). Ainley (2002) summarized the annual cycle.
Breeding Adélie penguins begin to arrive at Ross
Island colonies in late October, with females typically
laying 2 eggs by mid-November. Chicks hatch in
mid-December and remain at the colony until midFebruary. One parent remains with the chick(s) during the guard stage while the second parent forages
at sea. Parents switch roles every 1 to 3 d, with chicks
fed small meals by the guarding parent. Once chicks
are approximately 3 wk old, they are left unguarded
and begin to crèche (form groups of chicks independent of nests) as both parents need to forage to provide
sufficient food. Chicks typically fledge when they are
7 to 8 wk old. Our study period included most of
chick-rearing, from the early guard stage (late December) through late crèche (late January), for 15
austral summers (1996−1997 to 2010−2011). Hereafter, we refer to austral summers using the initial
year (i.e. 1996 refers to the breeding season beginning in October 1996 and ending in February 1997).
Weighing and measuring chicks
Once a week, beginning on 26 December at Cape
Bird and between 1 and 3 January at Capes Crozier
and Royds and ending 23 to 28 January, we selected
approximately 50 Adélie penguin chicks (25 at the
much smaller Royds) for inclusion in the study.
Whitehead et al.: Factors affecting Adélie penguin chicks
Chicks were selected randomly, with different parts
of the colonies used during each sampling period;
thus no chick was measured twice. During the first
2 wk chicks were in nests, and thereafter more and
more chicks were in crèches. When 2 chicks were
present in a nest, both chicks were captured for
measurement, and their sibling status recorded. Captured chicks were weighed and had their left flipper
measured before being returned to the nest or
crèche. Sampling ended once 50 individuals had
been processed. The actual age of sampled chicks
was not known. Instead, we estimated the approximate age of chicks in each sampling period relative
to the estimated date when 50% of nests within
closely monitored reference colonies had hatched.
Estimates of the median hatch date were calculated
separately for each breeding season and colony and
ranged from 13 December to 1 January, with chicks
typically hatching first at Cape Crozier, then Cape
Bird and finally Cape Royds (Dugger et al. 2014).
Thus, the median age of chicks in a given sampling
period is estimated in weeks since peak hatch
(‘week’).
Calculating chick condition
We calculated chick condition using the Scaled
Mass Index (SMI), a robust condition index that
accounts for differences in the ratio of size to mass
that may occur at different body sizes and which may
be functionally important independent of an individual’s energy stores (Peig & Green 2009). In this study
we use flipper length as a proxy for skeletal size. We
performed a standardised major axis regression
(SMA) on log-transformed mass and flipper length.
Then we used the slope from this regression to calculate condition using:
F b SMA
SMIi = M i ⎡ 0 ⎤
⎢⎣ Fi ⎥⎦
(1)
where Mi and Fi are the body mass and flipper
length, respectively, of individual i, bSMA is the slope
of the SMA regression of M on F, and F0 is the mean
flipper length of all sampled chicks. Therefore, the
condition score of an individual chick (SMIi) is their
predicted body mass (g) when their flipper length
has been standardized to F0. High condition scores
indicated individuals that were considered to be in
good condition (i.e. they are heavier in mass than
predicted for their structural size).
For all nests that contained 2 chicks at the time of
measurement, we randomly selected the data from
203
1 chick to ensure there were no issues of dependence
in the statistical analyses. In addition, we calculated
the absolute differences in sibling size (sizesib), mass
(masssib) and condition (conditionsib) for each nest.
Siblings could not be identified once chicks reached
the crèche stage.
Biotic explanatory variables
Parameters relating to adult provisioning efficiency
at each of the 3 colonies were estimated from a small
subcolony (~200 pairs) enclosed by a fence, where
the only access in and out was over an automated
weighbridge system consisting of a scale, direction
sensor, and radio-frequency identification reader
connected to a data logger (see Ballard et al. 2001 for
more details). A subset of breeding individuals (25 to
59 individuals at Cape Crozier, 3 to 93 at Cape Bird,
and 16 to 74 at Cape Royds, depending on breeding
season) within each of these subcolonies were
implanted with passively integrated transponders,
providing unique identification. If sample size was
low at the beginning of a breeding season, we implanted transponders in additional, randomly selected individuals as needed. Each time a penguin
crossed the weighbridge, the bird identification, date
and time, direction of travel, and body mass were
recorded automatically (Ballard et al. 2001). These
data provided a measure of the frequency with which
parents visited their chicks as well as the amount of
food delivered, allowing the calculation of provisioning efficiency. For each parental foraging trip, provisioning efficiency was calculated as the amount of
food (g) brought back to the colony by an adult (calculated as a parent’s incoming mass minus its mass
on the subsequent departure, i.e. including both the
food delivered to the chicks and the food digested by
the adult when attending the nest) divided by the
duration of the foraging trip (min) (also referred to as
catch per unit effort in previous publications; see Ballard et al. 2010, Lescroël et al. 2010, 2014 for more
details). As the latter studies note, over the course of
the breeding season parent mass does change, but
not radically within the time of a single foraging trip.
Parents that return quickly from foraging feed their
chicks more often (Salihoglu et al. 2001, Chapman et
al. 2011). This is especially true once chicks are in the
crèche, with parents returning to sea immediately
after feeding their chick(s) once, rather than small
sequential feeds when guarding smaller chicks.
These data were summarised to provide a weekly
mean estimate of provisioning efficiency for each
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breeding season and colony corresponding to the
same time periods in which the chicks were measured. Provisioning efficiency data were only available from 1996 through 2006.
Diet composition was estimated using data obtained by multiple methods: (1) stomach flushing
samples (1996 to 2005; n = 4 to 56 colony−1 breeding
season−1), (2) observing chick feeding events using
binoculars to assess prey species (fish: grey colour;
krill: pink) passed from adult to chick (2001 to 2010;
n = 2 to 541 colony−1 breeding season−1), (3) dissecting the stomachs of chicks killed by south polar skuas
Stercorarius maccormicki (2000 to 2010; n = 1 to 78
colony−1 breeding season−1), and (4) noting food spilt
around nests (2000 to 2010; n = 1 to 95 colony−1
breeding season−1) (see Ainley et al. 2003, 2006 for
further details). The stomach sampling and chick
stomach dissections indicated that > 95% of the diet
was composed of Antarctic silverfish and crystal krill,
making the more general results of the visual sampling suitable for our purposes (approximate proportion of fish vs. krill, also confirmed by stable isotope
analysis of chick tissues: Ainley et al. 2003). These
data were summarised to provide a weekly mean
approximation of the proportion of fish (‘fish’) in the
diet for each breeding season and colony.
The mean number of chicks produced per pair at
each colony was estimated each breeding season as a
measure of breeding output (Dugger et al. 2014). The
number of breeding pairs on active nests in a specified set of subcolonies was counted during late incubation (25 November to 8 December), when a minimum number of adults are present (Taylor et al. 1990,
Ainley 2002). We then counted the number of chicks
present in the same subcolonies once most chicks
had entered crèche (15 to 20 January). Breeding output in each subcolony was calculated as the ratio of
chicks to active nests, with mean values estimated for
each colony in each breeding season (‘breeding output’).
We used aerial photography to estimate the number of occupied territories present at each colony
(‘colony size’; Lyver et al. 2014). The colonies were
overflown by helicopter and photographed; the
resulting images were of sufficient resolution to
clearly identify individual penguins. Flights were
carried out within a few days of 1 December (depending on weather; 25 November to 8 December)
when the population was composed of single birds
incubating eggs and very few non-breeders (Taylor
et al. 1990, Ainley 2002). The number of occupied
territories were counted to provide an index of the
breeding pairs present at the colony.
Abiotic explanatory variables
Sea ice concentration (SIC) was calculated as the %
ice cover within the potential foraging area of each
colony (Ballard et al. 2010) as measured weekly by
passive microwave imagery using the Special Sensor
Microwave/Image (SSMI, Cavalieri & Comiso 2004).
The potential foraging area was determined as the
polygon that contained 95% of at-sea positions of provisioning parents as determined by radio and satellite
telemetry from 1997 to 2006 (Ainley et al. 2004, 2006,
D. G. Ainley unpubl. data). These are shown visually
in Dugger et al. (2014) and Ford et al. (2014). The area
that the giant icebergs (B-15 and C-16; Robinson &
Williams 2012) occupied within the foraging area was
omitted from the SIC calculation because this area
was never available for foraging, and because the
presence/absence of the giant icebergs in each
breeding season was accounted for using a separate
explanatory variable. The icebergs did not arrive until
after the crèche period in the 2000 breeding season
(see maps in Ainley et al. 2004, Shepherd et al. 2005,
Ballard et al. 2010), thus we considered this breeding
season to be a ‘non-iceberg season’. The icebergs departed in July 2006, and thus 2006 was the first breeding season free of their presence.
Statistical analyses
Our specific predictions were tested by evaluating
the relationships between dependent and explanatory variables (Table 1) using mixed effects models
constructed with the ‘nlme’ package (Pinheiro et al.
2012) in R v.2.15.0 (R Development Core Team 2012).
Further details of the specific predictions and models
are given below and in Table 2. Prior to analysis, we
assessed the relationships between all explanatory
variables to ensure that they were not correlated. We
examined all possible additive combinations of the
fixed explanatory variables for each prediction using
the ‘MuMIn’ package (Barton 2012), ranking the
models by their corrected Akaike’s Information Criterion (AICc ) score. Models within 2 AICc (Δi ) of the
best model value (referred to herein as the top model
set) were deemed to be potentially relevant and
examined for alternate explanations. Given that different combinations of parameters may have varying
ecological interpretations, we only report effect sizes
for the best fitting model (i.e. the lowest AICc score)
rather than model-averaged estimates, thus identifying the best combination of parameters that described each dependent variable. Due to the diffi-
Whitehead et al.: Factors affecting Adélie penguin chicks
205
Table 1. Parameters measured and included in models describing Adélie penguin chick condition and mass on Ross Island. Means ± SE and
ranges for the earliest to latest weekly measurements are calculated across all colonies and breeding seasons. Further information about
how each parameter was calculated is provided in ‘Materials and methods’
Parameter
Response variables
Size
Mass
Condition
Sizesib
Masssib
Conditionsib
Description
Mean ± SE (Range)
Flipper length of Adélie penguin chicks (mm)
Mass of Adélie penguin chicks (g)
Condition of Adélie penguin chicks calculated using
the scaled mass index, SMI (g)
Difference in flipper length between siblings from the same nest (mm)
Difference in mass between siblings from the same nest (g)
Difference in condition between siblings from the same nest (g)
138.7 ± 0.5 (25, 216)
1984.8 ± 12.3 (50, 5000)
1789.1 ± 3.8 (786, 2803)
14.7 ± 0.4 (0, 77)
256.1 ± 7.0 (0, 1400)
270.7 ± 7.6 (0, 1986)
Food availability and quality
Provisioning efficiency
Mean catch per unit effort at each colony per week (g min−1)
Fish
Mean proportion of the diet comprised of silverfish per week (%)
0.46 ± 0.003 (0.02, 1.58)
43.8 ± 0.4 (0.0, 100.0)
Competition
Colony size
Breeding output
Number of breeding pairs present at each colony each breeding season
Mean number of chicks produced per pair in each breeding season
(chicks pair−1)
65 270 ± 8409 (1367, 282 515)
0.89 ± 0.07 (0.06, 1.56)
SIC per week (% of foraging area at each colony covered by sea ice)
Y/N, whether giant icebergs were present
33.5 ± 2.2 (0.0, 99.8)
Present: 2001−2005
Environmental conditions
Sea ice concentration (SIC)
Iceberg
Table 2. Predictions regarding relationships between dependent variables and covariates for Adélie penguin chicks at 3 colonies on Ross
Island, Antarctica. Detailed explanations of the parameters are given in Table 1 and ‘Materials and methods’
General prediction
Specific prediction:
dependent
variables
Predicted effects
1. Chick size and mass will be greater, and
1.1 Size
condition better, when provisioning efficiency
1.2 Mass
is high, SIC is low and fish are dominant in the diet 1.3 Condition
βprovisioning efficiency > 0
βfish > 0
βln(SIC) < 0
βage > 0
βcolony (variable)
βcolony × βln(SIC) (variable)
Random variable: week since peak hatch|breeding season
2. Chick size and mass will be greater, and
condition better, in breeding seasons with low
intraspecific resource competition
2.1 Size
2.2 Mass
2.3 Condition
βiceberg < 0
βcolony size < 0
βbreeding output < 0
Random variable: week since peak hatch
3. Siblings will be most similar in size, mass
and condition, in breeding seasons with low
intraspecific resource competition
3.1 Sizesib
3.2 Masssib
3.3 Conditionsib
βiceberg < 0
βcolony size < 0
βbreeding output < 0
Random variable: week since peak hatch
culty in correctly estimating residual degrees of freedom in mixed effects models, we used 95% confidence intervals, and whether or not they included
zero, to evaluate strength and direction of effects
(Bolker et al. 2009). Throughout this paper, all means
are provided ± SE.
Prediction 1: Chick size (1.1) and mass (1.2) will be
greater, and condition (1.3) will be better when provisioning efficiency is high, SIC is low and fish are dom-
inant in the diet. We evaluated whether chick size,
mass and condition varied weekly with the adult provisioning efficiency and diet quality (‘fish’), as well as
the role of SIC (ln[SIC]) and SIC–colony interactions
(ln[SIC]:colony), in modifying the relationships. We
included week since peak hatch within breeding
season as a random effect. These analyses were restricted to data collected between 1998 and 2006 due
to missing data in the provisioning efficiency dataset.
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Prediction 3: Sibling chicks will be most similar in
size (3.1), mass (3.2) and condition (3.3) in breeding
seasons with low intraspecific resource competition.
We evaluated whether differences in sibling size,
mass and condition varied between breeding seasons
using colony size, breeding output and iceberg presence used as proxies for resource competition. We
included week as a random effect to account for variable peak hatch date.
RESULTS
Fig. 2. Mean weekly relationships between (a) size (as measured by flipper length), (b) mass and (c) condition of Adélie
penguin chicks. Data are summarised by age (week since
peak hatch) across all breeding seasons sampled. Error bars:
± SE. Further details on each of the metrics can be found in
Table 1 and ‘Materials and methods’
Prediction 2: Chick size (2.1) and mass (2.2) will be
greater, and condition (2.3) will be better in breeding
seasons with low intraspecific resource competition.
We evaluated how chick size, mass and condition
varied between breeding seasons, using colony size,
breeding output and iceberg presence as proxies for
resource competition among parents. We included
week as a random effect to account for variable peak
hatch date.
A total of 8693 Adélie penguin chicks were weighed and measured among the 3 colonies on Ross
Island between 1 January 1997 and 28 January 2011
(Royds: 1801, Bird: 3588, Crozier: 3304). Chick mass
ranged from 50 to 5000 g (mean ± SE: 1758.0 ± 18.3 g)
over the length of the breeding season, while size
(measured as flipper length) varied from 25 to
216 mm (138.7 ± 0.5 mm; Table 1, Fig. 2). Using the
mean flipper length as F0 , our estimates of condition
based on the SMI ranged from 786 to 2803 g (1733.8
± 6.8 g) over the entire breeding season. Just prior to
fledging when chicks were approximately 5 wk old,
chick size ranged from 71 to 216 mm (176 ± 0.4 mm),
with chicks being a similar size at all 3 colonies
(Fig. 2). Chick mass varied from 500 to 4850 g (2589 ±
17.2 g), with chicks notably smaller at Cape Crozier
than the other sites. Similarly, chick condition at 6 wk
was lowest at Cape Crozier and highest at Cape
Royds, with condition pooled across the sites ranging
from 806 to 2801 g (1761 ± 7.4).
Prediction 1.1: Chick size will be greater when provisioning efficiency is high, SIC is low and fish are
dominant in the diet. Chick size varied among
colonies, with chicks smaller for their age at Cape
Crozier compared with Capes Bird and Royds
(Table 3). Chick size was negatively correlated with
ln(SIC), with this effect strongest at Cape Bird and
Cape Royds. The proportion of fish in the diet had a
positive effect on chick size, independent of the fact
that a greater proportion of the diet was composed of
fish later in the breeding season when chicks were
necessarily larger. Provisioning efficiency had a positive effect on chick size in several competitive models (< 2 AICc ) but was not included in the best model
(see the Appendix).
Prediction 1.2: Chick mass will be greater when
provisioning efficiency is high, SIC is low and fish are
dominant in the diet. (Fig. 2, Table 3). There was a
negative relationship between chick mass and
ln(SIC), and this relationship was strongest at Cape
Whitehead et al.: Factors affecting Adélie penguin chicks
ied between colonies, being positive
at Crozier and Bird but constant at
Royds. In contrast to our predictions,
there was a negative relationship
between chick condition and provisioning efficiency, with chicks in
poorer condition when provisioning
95% CI
efficiency was high. The proportion
86.86, 114.07
of fish in the diet had a positive ef−16.09, −10.35
fect on chick condition in the second
0.002, 0.124
best model (AICc = 1.08) but was not
51.55, 69.55
54.14, 78.02
included in the best model (Appen−15.68, −6.86
dix, Table 3).
−13.64, −2.89
Prediction 2.1: Chick size will be
420.93, 1068.1
greater in breeding seasons with
−43.49, −26.44
959.22, 1408.95
low intraspecific resource compe1043.36, 1544.95
tition. Mean chick size varied
15.16, 28.23
among breeding seasons in re18.32, 33.50
sponse to the presence of the giant
1805.16, 1987.08
−505.25, −290.8
icebergs, colony size and breeding
−361.30, −68.48
output (Appendix, Table 3). As pre42.48, 107.30
dicted, chicks were smaller at larger
−329.31, −61.39
53.87, 170.03
colonies (Fig. 3a) and in the pres−125.96, 11.65
ence of the icebergs (Fig. 4a). How96.67, 181.18
ever, in contrast to our predictions,
−11.42, −8.21
high breeding output was associ−0.00012, −0.00011
1.51, 5.42
ated with larger chicks (Table 3).
1130.90, 3036.20
Prediction 2.2: Chick mass will be
−384.73, −302.27
greater in breeding seasons with
−0.0033, −0.0030
low intraspecific resource compe−177.86, −77.66
tition. Mean chick mass varied
1761.07, 1879.50
−109.60, −62.49
among breeding seasons in re−202.42, −146.31
sponse to the presence of the giant
10.27, 17.48
icebergs, colony size and breeding
2.16, 5.97
output (Appendix, Table 3). As pre200.51, 399.20
dicted, chicks were lighter at larger
−74.24, −15.68
colonies (Fig. 3b) and when breed216.31, 306.10
0.00013, 0.00048
ing output was high, while the presence of the icebergs reduced mean
chick mass by 344 ± 21 g (Fig. 4b).
Prediction 2.3: Chick condition will be better in
breeding seasons with low intraspecific resource
competition. Mean chick condition varied among
breeding seasons in response to iceberg presence,
with chicks on average 77 ± 12 g lighter than expected for their body size when the icebergs were
present (Fig. 4c, Table 3). As predicted, high intraspecific competition negatively affected chick condition, with chicks in poorer condition when breeding
output was high (Appendix, Table 3). Colony size
had a negative impact on chick condition in the second best model (AICc = 0.47) but was not included in
the best model (see the Appendix).
Table 3. Estimates of parameter coefficients from the top model for each prediction. Detailed explanations of the parameters and predictions are given in Tables
1 & 2 and ‘Materials and methods’. For Models 1.1, 1.2, and 1.3, colony coefficients are presented relative to Cape Crozier, whose mean value for a given
dependent variable is therefore given by the intercept coefficient. SIC: Sea ice
concentration; Y: yes (i.e. iceberg present)
Model
Parameter
Coefficient
1.1 Size
Intercept
ln(SIC)
Fish
Colony = Bird
Colony = Royds
ln(SIC):colony = Bird
ln(SIC):colony = Royds
Intercept
ln(SIC)
Colony = Bird
Colony = Royds
ln(SIC):colony = Bird
ln(SIC):colony = Royds
Intercept
Colony = Bird
Colony = Royds
ln(SIC)
Provisioning efficiency
ln(SIC):colony = Bird
ln(SIC):colony = Royds
Intercept
Iceberg = Y
Colony size
Breeding output
Intercept
Iceberg = Y
Colony size
Breeding output
Intercept
Iceberg = Y
Breeding output
Intercept
Breeding output
Intercept
Iceberg = Y
Intercept
Colony size
100.46
6.94
−13.22
1.47
0.063
0.031
60.55
4.59
66.08
6.09
−11.27
2.25
−8.26
2.74
744.92
165.23
−34.96
4.35
1184.09
114.68
1294.15
127.90
21.70
3.33
25.91
3.87
1896.12
46.39
−398.02
54.68
−214.89
74.67
74.89
16.53
−195.35
68.32
111.95
29.62
−57.16
35.09
138.92
21.56
−9.81
0.82
−0.000113 0.000004
3.46
1.00
2083.55
485.97
−343.50
21.03
−0.0032
0.0001
−127.76
25.56
1820.29
30.21
−86.05
12.02
−174.37
14.31
13.87
1.84
4.06
0.97
299.85
50.62
−44.96
14.92
261.20
22.88
0.00024 0.00012
1.2 Mass
1.3 Condition
2.1 Size
2.2 Mass
2.3 Condition
3.1 Sizesib
3.2 Masssib
3.3 Conditionsib
SE
Royds and weakest at Cape Crozier. Several competitive models (AICc < 2) indicated that provisioning
efficiency had a negative relationship with chick
mass, while the proportion of fish in the diet was positively associated with chick mass. However, neither
variable was included in the best model (see the
Appendix).
Prediction 1.3: Chick condition will be better when
provisioning efficiency is high, SIC is low and fish are
dominant in the diet. Chick condition varied among
colonies, with chicks at Cape Crozier in better condition than those at Capes Bird and Royds (Fig. 2). The
relationship between chick condition and ln(SIC) var-
207
208
Mar Ecol Prog Ser 523: 199–213, 2015
source competition. The mean difference in the mass
of sibling chicks from the same nest was affected by
the presence of the giant icebergs (Table 3). Differences in sibling mass of up to 1400 g were observed,
with large differences in sibling mass less prevalent
when the icebergs were present (Fig. 4e). The breeding output and colony size were both included in several competitive models (AICc < 2; Appendix), with
high values of these variables tending to result in
greater differences in sibling mass.
Prediction 3.3: Sibling chicks will be most similar in
condition in breeding seasons with low intraspecific
resource competition. Differences in sibling condition were best explained by colony size, with greater
differences in sibling condition observed at larger
colonies (Appendix, Table 3). Iceberg presence and
breeding output were both included in several competitive models (AICc < 2; Appendix), with iceberg
presence and higher breeding output tending to
result in greater differences in condition between
sibling chicks.
DISCUSSION
Fig. 3. Relationship between colony size and (a) mean size
(as measured by flipper length), (b) mass and (c) condition of
Adélie penguin chicks. Data are summarised for chicks
approximately 5 wk old;. Error bars: ± SE. Further details on
each of the metrics can be found in Table 1 and ‘Materials
and methods’
Prediction 3.1: Sibling chicks will be most similar in
size in breeding seasons with low intraspecific resource competition. As predicted, variation in size
between sibling chicks from the same nest was
greater when breeding output was high (i.e. more
parents with 2-chick broods; Table 3). Iceberg presence was included in the second best mode (AICc =
0.61), with the difference in size between sibling
chicks tending to be smaller when the icebergs were
present (Fig. 4d, Appendix).
Prediction 3.2: Sibling chicks will be most similar in
mass in breeding seasons with low intraspecific re-
Our study clearly showed that the size, mass and
condition of Adélie penguin chicks varies with environmental conditions and intraspecific competition
among their parents, indicating that adult penguins
are unable to fully compensate and provide sufficient
resources during periods when assumed prey quality
and/or availability is low. Our results indicate that
altering the amount and quality of food (specifically
the proportion of fish) fed to chicks can affect growth,
as has previously been shown for Adélie penguins
(Salihoglu et al. 2001, Takahashi et al. 2003, Ballard
et al. 2010, Chapman et al. 2011) and other seabird
species (e.g. Wanless et al. 2005, Kitaysky et al.
2006). In fact, it appears that the inclusion of more
fish in the diet may offset reduced access to food (i.e.
when SIC is too high). This could be the reason we
did not detect a significant effect of provisioning efficiency on chick size and mass.
The major contribution of this study is the identification of mechanisms that drive provisioning and
growth of Adélie penguins chicks in the southern
Ross Sea, with both environmental conditions and
intraspecific competition shown to be important. Our
study indicates that the iceberg presence led to
smaller and lighter chicks, who were ultimately in
poorer condition (see also Ainley et al. 2004, Dugger
et al. 2014). While SIC increased at Capes Royds and
Bird due to iceberg presence, the location of the ice-
Whitehead et al.: Factors affecting Adélie penguin chicks
209
Fig. 4. Mean size, mass and condition of Adélie penguin chicks in the presence and absence of the giant icebergs. The left panels depict the mean (± SE) across all colonies at approximately 5 wk of age. The right panels depict the mean (± SE) difference
between individuals from the same nest at approximately 3 wk of age. Further details on each of the metrics can be found in
Table 1 and ‘Materials and methods’
bergs meant that foraging penguins at Cape Crozier
were prevented from foraging in the productive MIZ
of the Ross Sea Polynya, where they otherwise forage
in non-iceberg years (Dugger et al. 2014, Lescroël et
al. 2014). Thus, the mechanism by which iceberg
presence affected foraging differed between the
colonies, although the impacts on chick size, mass
and condition were similar. Adult Adélie penguins
are known to provide less food to chicks during periods of greater intraspecific competition (Ballard et al.
2010), as well as greater interspecific competition
(cetaceans; Ainley et al. 2006). Indeed, as colonies
grew in size (especially Cape Crozier) in the later
breeding seasons of our study, chick size and condition decreased. Chick size and condition were also
lower during breeding seasons of greater breeding
output when there is likely to be greater intraspecific
competition among foraging parents (Lewis et al.
2001). Overall, chicks tended to be larger but lighter
and in poorer condition when there was a greater
proportion of 2-chick broods (competition among
chicks). However, we also observed greater differences between sibling chicks in terms of size and
mass when there was a greater proportion of 2-chick
broods, despite the fact that Adélie penguins provide
more food to chicks in such nests (Ballard et al. 2010).
210
Mar Ecol Prog Ser 523: 199–213, 2015
Previous studies at Cape Crozier have shown that 6
to 15% SIC in the foraging range is optimal for foraging efficiency (and ultimately chick size and mass) in
this high latitude penguin species (Ballard et al. 2010,
Lescroël et al. 2010, 2014). This is consistent with penguins foraging in the MIZ of polynyas, where SIC rapidly increases with distance away from the polynya
edge (see Ainley et al. 1998). Sea ice concentration affects access to prey and possibly (but not necessarily)
prey abundance. The presence of the giant icebergs
led to increased SIC during those breeding seasons.
This was particularly evident close to Capes Royds
and Bird, although the proximity of Cape Crozier to
the Ross Sea Polynya meant that the SIC remained
relatively low during this period. As noted above, an
important effect of the icebergs on Cape Crozier penguins was blocked access to the MIZ.
Nest desertion was more common at Capes Royds
and Bird when SIC was high, probably because foraging trips took longer and mates were unable to
return before the brooding or guarding mate abandoned the nest to ensure its own survival (Ballard et
al. 2010). Thus, overall breeding success was lower in
these breeding seasons. What may have resulted was
essentially a selection for pairs in which both members had learned (or were predisposed) to forage in
nearby ice cracks in the otherwise almost complete
ice cover (D. G. Ainley pers. obs. at Royds and from
helicopter overflights). For those few pairs in which
both members foraged in cracks near the colony, the
chicks were well fed and were in better condition
than in non-iceberg breeding seasons. Clearly the ice
cracks would not have been able to support large
populations, with intraspecific competition for food
among adults likely high within a few largely enclosed spaces (Watanuki et al. 1993). Foraging in
cracks is common for the very small colony of Adélie
penguins (<1000 pairs) investigated by Watanuki et
al. (1993, 2003), a colony restricted in size due to poor
access to foraging habitat. Such a situation speaks
greatly to the power of polynyas for enhancing penguin colony size and even colony existence (Ainley
2002, Arrigo & van Dijken 2003).
Chick size and mass were lower during periods of
high SIC, with the greatest declines observed at
Cape Crozier. These relationships seem somewhat
counter-intuitive when considering SIC only. However, they become clearer when viewed in the context of intraspecific competition among foraging
parents. Most remarkable in our results was the fact
that the colonies at Cape Bird, and especially Cape
Crozier, began to increase in size after 2004, well
before the large icebergs departed in winter 2006,
and have continued to grow at an irregular rate in
subsequent breeding seasons (Lyver et al. 2014).
Accordingly, with the presumed increase in foraging
competition, chick size, mass and condition decreased at Cape Crozier. The pattern is counter-intuitive because decreased chick size and condition
should result in decreased probability of surviving
once chicks begin provisioning themselves (Perrins
et al. 1973, Coulson & Porter 1985, Magrath 1991,
Sagar & Horning 1998). Being quite speculative (but
under investigation using ocean glider studies), what
may be indicated is that despite food being depleted
close to colonies, food availability not far beyond the
colony ‘halo’ of intense foraging (Ballance et al. 2009)
was adequate for chicks to forage successfully postfledging. On the other hand, the time lag between
fledging and recruitment into the breeding population may mean that we have yet to see colony growth
be affected by a lower survival rate for chicks fledging in poor condition.
Increasing food availability beyond the colony foraging ‘halo’ could be a function of the decreased
prevalence of a major penguin competitor in the
southern Ross Sea. Large Antarctic toothfish, which
forage for silverfish in the water column (Eastman
1985), have disappeared in waters around Ross
Island, possibly the result of a fishery that has grown
since 1997 (Ainley et al. 2013). This reduction in
large toothfish may lead to an increase in the availability of energy-rich silverfish, which is likely to
result in larger Adélie penguin chicks (see also Salihoglu et al. 2001, Chapman et al. 2011) .
At present, we do not fully understand the demographic mechanisms that influence Adélie penguin
juvenile survival, particularly the effects of mass and
condition at fledging (but this is under investigation).
On average, near-fledging chicks from Cape Crozier
were ~700 g lighter than those from Cape Royds, yet
the Cape Crozier population has been exhibiting
rapid growth whereas Cape Royds has not. A fledgling with higher body condition (greater lipid and
protein reserves though structurally smaller) may
have greater fasting endurance and therefore more
potential to develop successful foraging strategies,
increasing their chances of survival (Millar & Hickling
1990, Schulte-Hostedde et al. 2001, Kitaysky et al.
2006). However, it is also possible that larger and
heavier chicks, such as those at Cape Royds, might be
less efficient foragers than their smaller counterparts
at Cape Crozier due to increased buoyancy. Underwater swimming speeds may be lower and required
dive depths more difficult to attain, with the ability to
evade predators also compromised. Alternatively,
Whitehead et al.: Factors affecting Adélie penguin chicks
even if provisioning is equal between different-sized
chicks, larger chicks may be at a disadvantage under
difficult foraging conditions due to their greater overall energetic requirements (Volkman & Trivelpiece
1980). If our research persists long enough to estimate
chick survival as a function of fledging size, mass and
condition (measurement of the mass of near-fledged
chicks at banding began in 2006), it may eventually
be possible to obtain sufficient data to identify links
between chick condition at fledgling, subsequent recruitment and trends in population size.
Understanding the relative effects of biotic and
abiotic drivers on population dynamics, and the interactions between them, is a key component in understanding the factors driving changes in animal
populations. We have shown that the size, mass and
condition of Adélie penguin chicks is greater during
times when environmental conditions allow for more
efficient parental foraging. In addition, we have
shown that in some cases, increased intraspecific
competition may be a more important driver of chick
size than abiotic factors. If we are to better understand the effects of climate change and altered food
web structures on penguins and other upper level
marine organisms, a more complete understanding
about how biotic and abiotic factors interact to influence population and ecosystem dynamics is required
(Estes 2014, Springer & van Vliet 2014).
Acknowledgements. A.L.W., P.O’B.L., B.J.K., K.B. and P.R.W.
were funded by New Zealand’s Foundation for Research,
Science and Technology (C09527, C09X0510) and Ministry
of Science and Innovation (C01X1001) and Landcare
Research grants, with logistic support from Antarctica New
Zealand. D.G.A., G.B., K.M.D., S.J. and A.L. were supported
by NSF grants (0440643 and 0944411), and the US Antarctic
Program. Our thanks go to the large number of field support
staff who assisted this study over the years. We also thank
M. Pinkerton, W. Fraser and the members of the New
Zealand Antarctic Fisheries Working Group for review of
the paper. All field work was conducted under a series of
Antarctic Conservation Act permits and NZ and US Animal
Ethic permits. Point Blue contribution #1994.
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213
Appendix. Model selection results for each prediction as evaluated by comparing corrected Akaike’s Information Criterion
(AICc). All possible combinations of terms that were included in each model set (different for each prediction; see Table 2)
were evaluated but only the models contributing 95% of the Akaike weights, as well as ‘intercept only’ models, are shown.
The model with the lowest AICc value for each prediction was chosen as the best model, and coefficients for the top model for
each prediction are reported in Table 3. The number of observations (n) and estimated parameters (K), differences in model
AICc value from the best model (ΔAICc) and Akaike weights (w) are shown for each model. Detailed explanations of the
parameters are given in Table 1 and ‘Materials and methods’
ΔAICc
Model
K
Log
likelihood
AICc
1.1 Size (n = 2689)
Colony + ln(SIC) + fish + ln(SIC):colony
Colony + ln(SIC) + provisioning efficiency + ln(SIC):colony
Colony + ln(SIC) + provisioning efficiency + fish +ln(SIC):colony
Colony + ln(SIC) + ln(SIC):colony
Intercept only
10
10
11
9
4
−12 439.3
−12 439.4
−12 438.8
−12 441.4
−12 559.1
24 898.65
24 898.97
24 899.67
24 900.79
25 126.25
0.00
0.33
1.02
2.14
227.6
0.358
0.304
0.215
0.123
0.000
1.2 Mass (n = 2689)
Colony + ln(SIC) + ln(SIC):colony
Colony + ln(SIC) + fish + ln(SIC):colony
Colony + ln(SIC) + provisioning efficiency + ln(SIC):colony
Colony + ln(SIC) + provisioning efficiency + fish + ln(SIC):colony
Intercept only
9
10
10
11
4
−20 813.9
−20 813.6
−20 813.9
−20 813.3
−20 894.3
41 645.82
41 647.19
41 647.78
41 648.61
41 796.53
0.00
1.38
1.96
2.79
150.71
0.471
0.237
0.176
0.117
0.000
1.3 Condition (n = 2689)
Colony + ln(SIC) + provisioning efficiency + ln(SIC):colony
Colony + ln(SIC) + provisioning efficiency + fish + ln(SIC):colony
Intercept only
10
11
4
−19 249.3
−19 248.9
−19 282.1
38 518.76
38 519.95
38 572.13
0.00
1.20
53.37
0.616
0.339
0.000
2.1 Size (n = 7011)
Breeding output + iceberg + colony size
Intercept only
6
3
−32 007.1
−32 593.8
64 026.26
65 193.51
0.00
1167.25
0.994
0.000
2.2 Mass (n = 7011)
Breeding output + iceberg + colony size
Intercept only
6
3
−54 758.0
−55 444.0
109 528.04
110 894.06
0.00
1366.02
1.000
0.000
2.3 Condition (n = 7011)
Breeding output + iceberg
Breeding output + iceberg + colony size
Intercept only
5
6
3
−50 856.3
−50 855.6
−50 931.5
101 722.65
101 723.12
101 868.96
0.00
0.47
146.31
0.558
0.442
0.000
3.1 Sizesib (n = 981)
Breeding output
Breeding output + iceberg
Breeding output + colony size
Breeding output + iceberg + colony size
Intercept only
4
5
5
6
3
−3815.7
−3815.0
−3815.7
−3815.0
−3824.4
7639.39
7640.00
7641.41
7642.02
7654.75
0.00
0.61
2.02
2.63
15.36
0.402
0.296
0.146
0.108
0.000
3.2 Masssib (n = 981)
Iceberg
Breeding output + iceberg
Breeding output
Iceberg + colony size
Breeding output + iceberg + colony size
Breeding output + colony size
Intercept only
4
5
4
5
6
5
3
−6689.5
−6688.6
−6689.7
−6689.3
−6688.5
−6689.6
−6694.0
13 386.94
13 387.17
13 387.45
13 388.56
13 389.01
13 389.21
13 393.95
0.00
0.23
0.50
1.62
2.06
2.26
7.01
0.260
0.232
0.202
0.116
0.093
0.084
0.008
3.3 Conditionsib (n = 981)
Colony size
Breeding output + colony size
Iceberg + colony size
Intercept only
Breeding output + iceberg + colony size
Breeding output
Iceberg
4
5
5
3
6
4
4
−6804.6
−6804.2
−6804.4
−6806.7
−6804.2
−6806.7
−6806.7
13 617.17
13 618.49
13 618.93
13 619.45
13 620.52
13 621.35
13 621.45
0.00
1.32
1.76
2.27
3.34
4.17
4.28
0.366
0.189
0.152
0.118
0.069
0.045
0.043
Editorial responsibility: Rory Wilson,
Swansea, UK
w
Submitted: May 21, 2014; Accepted: November 23, 2014
Proofs received from author(s): February 27, 2015